Morphology and porosity of the spines of the sea urchin Heterocentrotus mamillatus and their implications on the mechanical performance
Spines of the slate pencil sea urchin Heterocentrotus mamillatus Linnaeus, 1758, are in focus of biomimetic research as they feature a “graceful” failure behaviour under uniaxial compression dissipating energy and resisting high loads even after high strain. This study elucidates and quantifies the organization of calcitic trabeculae and pores in large primary spines of the slate pencil urchin H. mamillatus by image analysis from scanning electron microscopy, X-ray micro-computed tomography (µCT) and gravimetry. This study delivers a detailed distribution of porosities within the whole spine and shows that parts of the spines have a much higher porosity then hitherto thought. The central part (medulla) of the high-magnesium calcitic stereom of H. mamillatus spines has a porosity range of 75% to nearly 90%. From this innermost structure, more than 200 radially aligned, but often sinuous trabeculae extend to the spine rim. The structure of this complicated meshwork (radiating layer) is best seen in basal cross sections and was confirmed by µCT scans. The radiating layer has a porosity range from 40–70% and is irregularly separated by the dense growth layers (15–35% porosity). Growth layers were classified in proximal and distal growth layers with numbers ranging within a single animal between 3–14 and 2–7, respectively. These growth layers are characteristic for H. mamillatus spines and play a major role in their remarkable mechanical properties. The porosity of the spine increases from base to tip. Biological and mechanical implications of the variations are discussed.
KeywordsMorphology Echinoids Sea urchin spines Porosity µCT scans
The authors gratefully thank the German Research Foundation (DFG—Deutsche Forschungsgemeinschaft) for funding this work within the framework of the Collaborative Research Centre (SFB/Transregio) 141 “Biological Design and Integrative Structures” project B01. We also thank Barbara Maier and Simone Schafflick in the workshop for their support. The work of an anonymous reviewer is kindly appreciated.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
Statements on the welfare of animals
The sea urchins were purchased dead from a fossils collector, were not killed for the purpose of this study and are not listed as endangered species.
This article does not contain any studies with human participants performed by any of the authors.
- Clarke FW, Wheeler WC (1915) The inorganic constituents of echinoderms. US Geol Surv Prof Pap 90:191–196Google Scholar
- Deutler F (1926) Das Wachstum des Seeigelskeletts. In: Hartmann M, Hesse R (eds) Zoologische Jahrbücher Abteilung für Anatomie und Ontogenie der Tiere. Verlag von Gustav Fischer, Jena, pp 119–200Google Scholar
- Dotan A, Fishelson L (1985) Morphology of spines of Heterocentrotus mammillatus (Echinodermata: Echinoidae) and its ecological significance. In: Keegan BF, O‘Connor BDS (eds) Echinodermata: Proceedings of the international echinoderm conference, Galway 24–29 Sept 1984. A.A. Balkema, Rotterdam, pp 253–260Google Scholar
- Durham JW (1955) Classification of clypeasteroid echinoids. Univ Calif Press Geol Sci 31:73–198Google Scholar
- Ebert TA (1988) Growth, regeneration, and damage repair of spines of the slate-pencil sea urchin Heterocentrotus mammillatus. Pac Sci 42:160–172Google Scholar
- Emson RH (1985) Bone idle—a recipe for success? In: Keegan BF, O’Connor BDS (eds) Echinodermata. Balkema, Rotterdam, pp 25–30Google Scholar
- Grossmann JN, Nebelsick J (2013a) Stereom Differentiation in spines of Plococidaris verticillata, Heterocentrotus mammillatus and other regular sea urchins. In: Johnson C (ed) Echinoderms in a changing world. Taylor & Francis, London, pp 97–104Google Scholar
- Hasenpusch W (2000) Die Stachel der Griffelseeigel. Mikrokosmos 89:23–27Google Scholar
- Hesse E (1900) Die Mikrostruktur der fossilen Echinoidenstacheln und deren systematische Bedeutung. In: Bauer M, Koken E, Liebisch T (eds) Neues Jahrbuch für Mineralogie, Geologie und Paläontologie, E. Schweizertbart’sche Verlagshandlung, Stuttgart, pp 185–264Google Scholar
- Klang K, Bauer G, Toader N, Lauer C, Termin K, Schmier S, Kovaleva D, Haase W, Berthold C, Nickel KG, Speck T, Sobek W (2016) Plants and animals as source of inspiration for energy dissipation in load bearing systems and facades. In: Knippers J, Nickel KG, Speck T (eds) Biomimetic research for architecture and building construction. Springer, Switzerland, pp 109–133. https://doi.org/10.1007/978-3-319-46374-2_7
- Kroh A, Nebelsick JH (2010) Echinoderms and Oligo-Miocene Carbonate Systems: potential applications in sedimentology and environmental reconstruction. Int Assoc Sedimentol Spec Publ 42:201–228Google Scholar
- Lawrence JM (1987) A functional biology of echinoderms. The Johns Hopkins University Press, BaltimoreGoogle Scholar
- Nichols D (1962) Echinoderms. Anchor Press, Essex, p 200Google Scholar
- Presser V, Kohler C, Zivcová Z, Berthold C, Nickel KG, Schultheiß S, Gregorová E, Pabst W (2009b) Sea urchin spines as a model-system for permeable, light-weight ceramics with graceful failure behavior. Part II. Mechanical behavior of sea urchin spine inspired porous aluminum oxide ceramics under compression. J Bionic Eng 6:357–364CrossRefGoogle Scholar
- R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
- Schmier S, Lauer C, Schäfer I, Klang K, Bauer G, Thielen M, Termin K, Berthold C, Schmauder S, Speck T, Nickel KG (2016) Developing the experimental basis for an evaluation of scaling properties of brittle and ‘Quasi-Brittle’ biological materials. In: Knippers J, Nickel KG, Speck T (eds) Biomimetic research for architecture and building construction. Springer, Switzerland, pp 277–294. https://doi.org/10.1007/978-3-319-46374-2_14 CrossRefGoogle Scholar
- Simkiss K, Wilbur KM (1989) Echinoderms - cells and syncytia. Biomineralization: cell biology and mineral deposition. Harcourt Brace Jovanovich, San Diego, pp 146–149Google Scholar
- Smith A (1980) Stereom microstructures of the echinoid test. Spec Pap Palaeontol 25:1–81Google Scholar
- Telford M (1982) Echinoderm spine structure, feeding and host relationships of four species of dissodactylus (Brachyura: Pinnotheridae). Bull Mar Sci 32:584–594Google Scholar
- Vevers HG (1966) Pigmentation. In: Boolootian RA (ed) Physiology of Echinodermata. Interscience Publishers, New York, pp 265–267Google Scholar
- Weber JN (1969b) Origin of concentric banding in the spines of the tropical Echinoid Heterocentrotus. Pac Sci 23:452–466Google Scholar